Abstract

Macroparasite infections (e.g., helminths) remain a major human health concern. However, assessing transmission dynamics is problematic because the direct observation of macroparasite dispersal among hosts is not possible. We used a novel landscape genetics approach to examine transmission of the human roundworm Ascaris lumbricoides in a small human population in Jiri, Nepal. Unexpectedly, we found significant genetic structuring of parasites, indicating the presence of multiple transmission foci within a small sampling area (∼14 km2). We analyzed several epidemiological variables, and found that transmission is spatially autocorrelated around households and that transmission foci are stable over time despite extensive human movement. These results would not have been obtainable via a traditional epidemiological study based on worm counts alone. Our data refute the assumption that a single host population corresponds to a single parasite transmission unit, an assumption implicit in many classic models of macroparasite transmission. Newer models have shown that the metapopulation-like pattern observed in our data can adversely affect targeted control strategies aimed at community-wide impacts. Furthermore, the observed metapopulation structure and local mating patterns generate an excess of homozygotes that can accelerate the spread of recessive traits such as drug resistance. Our study illustrates how molecular analyses complement traditional epidemiological information in providing a better understanding of parasite transmission. Similar landscape genetic approaches in other macroparasite systems will be warranted if an accurate depiction of the transmission process is to be used to inform effective control strategies.

Highlights

  • Effective control of infectious diseases requires knowledge of transmission dynamics

  • Landscape genetic analyses can be used to test for correlations with ecological factors that may affect the distribution of genetic variation within and among these genetic clusters [8]

  • By incorporating the genetic clustering results with spatial, landscape, and epidemiological variables, one can highlight factors that affect parasite dispersal patterns. Such molecular epidemiological data can provide a detailed understanding of parasite transmission patterns even on very local scales [2]

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Summary

Introduction

Effective control of infectious diseases requires knowledge of transmission dynamics. Molecular markers and population genetic analyses provide a useful means to examine dispersal patterns [2,3]. For many human helminth infections, analyses based on multilocus genotypic data and population structure can provide a powerful alternative approach to elucidate transmission patterns. By incorporating the genetic clustering results with spatial, landscape, and epidemiological (e.g., host age, gender) variables, one can highlight factors that affect parasite dispersal patterns. Such molecular epidemiological data can provide a detailed understanding of parasite transmission patterns even on very local scales [2]

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